Cell - 8 September 2016

(Amelia) #1

NIH Grants AI100148 and AI109632 (M.C.N.); the International AIDS Vaccine
Initiative Neutralizing Antibody Consortium and Center (W.R.S. and D.R.B.);
CAVD funding for the IAVI NAC Center (W.R.S. and D.R.B.); the Ragon Institute
of MGH, MIT, and Harvard (W.R.S. and D.R.B.); The Robertson Foundation
and the Rockefeller University. A.E. was supported by an international post-
doctoral fellowship from the Clarin COFUND-Marie Curie program (PCTI-
FICYT). P.D. was supported by an international postdoctoral fellowship from
the Swedish Research Council. A.D.G. was supported by MSTP grant
T32GM07739 to the Weill Cornell/Rockefeller/Sloan-Kettering Tri-Institutional
MD-PhD Program. M.C.N. is a Howard Hughes Medical Institute Investigator.


Received: May 24, 2016
Revised: July 5, 2016
Accepted: July 20, 2016
Published: September 8, 2016


REFERENCES


Andrabi, R., Voss, J.E., Liang, C.H., Briney, B., McCoy, L.E., Wu, C.Y., Wong,
C.H., Poignard, P., and Burton, D.R. (2015). Identification of common features
in prototype broadly neutralizing antibodies to HIV envelope V2 apex to facil-
itate vaccine design. Immunity 43 , 959–973.
Baumjohann, D., Preite, S., Reboldi, A., Ronchi, F., Ansel, K.M., Lanzavecchia,
A., and Sallusto, F. (2013). Persistent antigen and germinal center B cells sus-
tain T follicular helper cell responses and phenotype. Immunity 38 , 596–605.


Bhiman, J.N., Anthony, C., Doria-Rose, N.A., Karimanzira, O., Schramm, C.A.,
Khoza, T., Kitchin, D., Botha, G., Gorman, J., Garrett, N.J., et al. (2015). Viral
variants that initiate and drive maturation of V1V2-directed HIV-1 broadly
neutralizing antibodies. Nat. Med. 21 , 1332–1336.
Bonsignori, M., Hwang, K.K., Chen, X., Tsao, C.Y., Morris, L., Gray, E.,
Marshall, D.J., Crump, J.A., Kapiga, S.H., Sam, N.E., et al. (2011). Analysis
of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific
broadly neutralizing antibodies and their inferred unmutated common ances-
tors. J. Virol. 85 , 9998–10009.
Burton, D.R., and Hangartner, L. (2016). Broadly neutralizing antibodies to HIV
and their role in vaccine design. Annu. Rev. Immunol. 34 , 635–659.
Burton, D.R., Desrosiers, R.C., Doms, R.W., Koff, W.C., Kwong, P.D., Moore,
J.P., Nabel, G.J., Sodroski, J., Wilson, I.A., and Wyatt, R.T. (2004). HIV vaccine
design and the neutralizing antibody problem. Nat. Immunol. 5 , 233–236.
Cohen, Y.Z., and Dolin, R. (2013). Novel HIV vaccine strategies: overview and
perspective. Ther. Adv. Vaccines 1 , 99–112.
Dimitrov, D.S. (2010). Therapeutic antibodies, vaccines and antibodyomes.
MAbs 2 , 347–356.
Doria-Rose, N.A., Schramm, C.A., Gorman, J., Moore, P.L., Bhiman, J.N.,
DeKosky, B.J., Ernandes, M.J., Georgiev, I.S., Kim, H.J., Pancera, M., et al.;
NISC Comparative Sequencing Program (2014). Developmental pathway for
potent V1V2-directed HIV-neutralizing antibodies. Nature 509 , 55–62.
Dosenovic, P., von Boehmer, L., Escolano, A., Jardine, J., Freund, N.T., Gitlin,
A.D., McGuire, A.T., Kulp, D.W., Oliveira, T., Scharf, L., et al. (2015). Immuni-
zation for HIV-1 broadly neutralizing antibodies in human Ig knockin mice.
Cell 161 , 1505–1515.
Eda, Y., Takizawa, M., Murakami, T., Maeda, H., Kimachi, K., Yonemura, H.,
Koyanagi, S., Shiosaki, K., Higuchi, H., Makizumi, K., et al. (2006). Sequential
immunization with V3 peptides from primary human immunodeficiency virus
type 1 produces cross-neutralizing antibodies against primary isolates with a
matching narrow-neutralization sequence motif. J. Virol. 80 , 5552–5562.
Foote, J., and Eisen, H.N. (1995). Kinetic and affinity limits on antibodies pro-
duced during immune responses. Proc. Natl. Acad. Sci. USA 92 , 1254–1256.
Garces, F., Sok, D., Kong, L., McBride, R., Kim, H.J., Saye-Francisco, K.F.,
Julien, J.P., Hua, Y., Cupo, A., Moore, J.P., et al. (2014). Structural evolution
of glycan recognition by a family of potent HIV antibodies. Cell 159 , 69–79.
Garces, F., Lee, J.H., de Val, N., de la Pena, A.T., Kong, L., Puchades, C., Hua,
Y., Stanfield, R.L., Burton, D.R., Moore, J.P., et al. (2015). Affinity maturation of


a potent family of HIV antibodies is primarily focused on accommodating or
avoiding glycans. Immunity 43 , 1053–1063.
Gautam, R., Nishimura, Y., Pegu, A., Nason, M.C., Klein, F., Gazumyan, A.,
Golijanin, J., Buckler-White, A., Sadjadpour, R., Wang, K., et al. (2016). A single
injection of anti-HIV-1 antibodies protects against repeated SHIV challenges.
Nature 533 , 105–109.
Gonza ́lez-Ferna ́ndez, A., and Milstein, C. (1998). Low antigen dose favours
selection of somatic mutants with hallmarks of antibody affinity maturation.
Immunology 93 , 149–153.
Goodnow, C.C., Vinuesa, C.G., Randall, K.L., Mackay, F., and Brink, R. (2010).
Control systems and decision making for antibody production. Nat. Immunol.
11 , 681–688.
Gorman, J., Soto, C., Yang, M.M., Davenport, T.M., Guttman, M., Bailer, R.T.,
Chambers, M., Chuang, G.Y., DeKosky, B.J., Doria-Rose, N.A., et al.; NISC
Comparative Sequencing Program (2016). Structures of HIV-1 Env V1V2
with broadly neutralizing antibodies reveal commonalities that enable vaccine
design. Nat. Struct. Mol. Biol. 23 , 81–90.
Gray,E.S., Madiga, M.C., Hermanus, T., Moore, P.L., Wibmer, C.K., Tumba,
N.L., Werner, L., Mlisana, K., Sibeko, S., Williamson, C., et al.; CAPRISA002
Study Team (2011). The neutralization breadth of HIV-1 develops incrementally
over four years and is associated with CD4+ T cell decline and high viral load
during acute infection. J. Virol. 85 , 4828–4840.
Gruell, H., Bournazos, S., Ravetch, J.V., Ploss, A., Nussenzweig, M.C., and
Pietzsch, J. (2013). Antibody and antiretroviral preexposure prophylaxis pre-
vent cervicovaginal HIV-1 infection in a transgenic mouse model. J. Virol. 87 ,
8535–8544.
Haynes, B.F., and Montefiori, D.C. (2006). Aiming to induce broadly reactive
neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev.
Vaccines 5 , 347–363.
Haynes, B.F., Kelsoe, G., Harrison, S.C., and Kepler, T.B. (2012). B-cell-line-
age immunogen design in vaccine development with HIV-1 as a case study.
Nat. Biotechnol. 30 , 423–433.
Hoot, S., McGuire, A.T., Cohen, K.W., Strong, R.K., Hangartner, L., Klein, F.,
Diskin, R., Scheid, J.F., Sather, D.N., Burton, D.R., and Stamatatos, L.
(2013). Recombinant HIV envelope proteins fail to engage germline versions
of anti-CD4bs bNAbs. PLoS Pathog. 9 , e1003106.
Hraber, P., Seaman, M.S., Bailer, R.T., Mascola, J.R., Montefiori, D.C., and
Korber, B.T. (2014). Prevalence of broadly neutralizing antibody responses
during chronic HIV-1 infection. AIDS 28 , 163–169.
Jardine, J., Julien, J.P., Menis, S., Ota, T., Kalyuzhniy, O., McGuire, A., Sok, D.,
Huang, P.S., MacPherson, S., Jones, M., et al. (2013). Rational HIV immu-
nogen design to target specific germline B cell receptors. Science 340 ,
711–716.
Jardine, J.G., Ota, T., Sok, D., Pauthner, M., Kulp, D.W., Kalyuzhniy, O., Skog,
P.D., Thinnes, T.C., Bhullar, D., Briney, B., et al. (2015). HIV-1 VACCINES.
Priming a broadly neutralizing antibody response to HIV-1 using a germline-
targeting immunogen. Science 349 , 156–161.
Jardine, J.G., Kulp, D.W., Havenar-Daughton, C., Sarkar, A., Briney, B., Sok,
D., Sesterhenn, F., Eren ̃o-Orbea, J., Kalyuzhniy, O., Deresa, I., et al. (2016).
HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-tar-
geting immunogen. Science 351 , 1458–1463.
Julien, J.P., Sok, D., Khayat, R., Lee, J.H., Doores, K.J., Walker, L.M., Ramos,
A., Diwanji, D.C., Pejchal, R., Cupo, A., et al. (2013). Broadly neutralizing anti-
body PGT121 allosterically modulates CD4 binding via recognition of the HIV-1
gp120 V3 base and multiple surrounding glycans. PLoS Pathog. 9 , e1003342.
Kepler, T.B. (2013). Reconstructing a B-cell clonal lineage. I. Statistical infer-
ence of unobserved ancestors. F1000Res. 2 , 103.
Kepler, T.B., Liao, H.X., Alam, S.M., Bhaskarabhatla, R., Zhang, R., Yandava,
C., Stewart, S., Anasti, K., Kelsoe, G., Parks, R., et al. (2014). Immunoglobulin
gene insertions and deletions in the affinity maturation of HIV-1 broadly reac-
tive neutralizing antibodies. Cell Host Microbe 16 , 304–313.
Klein, F., Halper-Stromberg, A., Horwitz, J.A., Gruell, H., Scheid, J.F., Bourna-
zos, S., Mouquet, H., Spatz, L.A., Diskin, R., Abadir, A., et al. (2012). HIV

1456 Cell 166 , 1445–1458, September 8, 2016

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